Emotion-induced changes in human medial prefrontal cortex: I. During cognitive task performance

Abstract

Regional cerebral blood flow (BF) was examined in regions of the medial prefrontal cortex (MPFC) with positron-emission tomography while subjects performed two cognitive tasks, reading nouns aloud and generating appropriate verbs for the same nouns. The control task was passive viewing of the same words. BF was reduced in regions of the MPFC during word reading and naive verb generation, relative to a control state in which the subjects passively viewed nouns. Practicing verb generation produced improved performance, as measured by response time, which was strongly correlated with further reductions in MPFC and hypothalamic BF. After practice, when verb generation was performed on a novel list of words, reaction times slowed and the pattern of MPFC BF reverted to that seen in the word reading and naive conditions. A separate behavioral study of the verb-generation task indicated that anxiety, high during naive use-generation as measured by heart rate and self-report, decreased with practice on the task but returned with the introduction of a novel list of words. Taken together, these results suggest that the MPFC is part of a network, including the hypothalamus and brainstem, whose activity reflects a dynamic interplay between cognitive task performance and emotion.

Figure 1

(A) Response times (means ± SEM) across verb generation trials in 12 subjects generating appropriate verbs while in a PET scanner. PET scans were performed during the naïve, practiced, and novel blocks. (B) Response times (n = 15); (C) visual analog scale rating of anxiety (n = 15); and (D) heart rate (n = 7) measurements for the behavioral study of the verb generation task. All measurements are means ± SEM. Block 0 is reading nouns, block 1 is the first (naïve) verb generation block, and block 11 is verb generation with a novel list of nouns.

Figure 2

(Left) Averaged subtraction PET images in atlas space (48) for each of the conditions examined. Upper Left, reading nouns aloud; Upper Right, naïve verb generation; Lower Left, practiced verb generation; and Lower Right, verb generation on a novel list of nouns. All comparisons are to passive viewing of nouns. Each image is a sagittal section taken 1 mm to the right of the midsaggital plane. Anterior is to the left. The color scale is a linear scale of normalized radioactive counts. The locations of the three MPFC regions studied are indicated with pink circles on each image. The ROIs are referred to by the BA originally assigned to them by Shulman and colleagues: BA 8/9 located at x = 5, y = 49, z = 36; BA 10 located at x = −1, y = 47, z = −4; and BA 32 located at x = 3, y = 31, z = −10. We note BA 32 most likely includes the adjacent BA 24 and 25 as well. (Right) Relative blood flow change (means ± SEM) in normalized counts within each region for each of the four comparisons: read = black bar; naïve = diagonal stripe bar; practiced = clear bar; and novel = horizontal stripe bar.

Figure 3

Relative blood flow change in the BA 32 region (see Fig. 1) in the practiced minus the naïve verb generation condition compared with the response time improvement occurring as the result of practice on the task (r = −0.85 and P < 0.0005).